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MARINE ECOLOGY PROGRESS SERIES

Mar Ecol Prog SerVol. 535: 11-27, 2015

doi: 10.3354/meps11429

Published September 15

INTRODUCTION

Marine ecosystems, in particular phototrophic

components of the pelagic microbial food web

(MFW), fix nearly half of the total global carbon(Field et al. 1998) and have a major effect on global

climate, particularly in the context of climate change and increasing atmospheric CO2 with its conse- quences such as global warming and ocean acidifi- cation. There are continuous interactions among © Inter-Research 2015 · www.int-res.com*Corresponding author: behzad.mostajir@cnrs.fr

Microbial food web structural and functional

responses to oyster and fish as top predators

Behzad Mostajir

1, *, Cécile Roques 1 , Corinne Bouvier 1 , Thierry Bouvier 1

Éric Fouilland1

, Patrice Got 1 , Emilie Le Floc'h 1 , Jean Nouguier 1 , Sébastien Mas 2

Richard Sempéré

3 , Télesphore Sime-Ngando 4 , Marc Troussellier 1 , Francesca Vidussi 1 1

Center of Marine Biodiversity, Exploitation and Conservation, UMR 9190, CNRS/Université de Montpellier/IRD/IFREMER,

Place Eugène Bataillon, Université de Montpellier, Case 93, 34095 Montpellier Cedex 05, France2

Observatoire de Recherche Méditerranéen de l'Environnement, UMS 3282,

Centre d'Ecologie Marine Expérimentale MEDIMEER, Station Méditerranéenne de l'Environnement Littoral, Université de

Montpellier/CNRS/IRD, Place Eugène Bataillon, Université de Montpellier, Case 60, 34095 Montpellier Cedex 05, France

3

Aix-Marseille Université, Mediterranean Institute of Oceanography (UMR 7294), CNRS/IRD, Aix Marseille University,

Toulon University, Case 901, Campus de Luminy, Bâtiment Méditerranée, 13288 Marseille Cedex 9, France

4

Laboratoire Microorganismes: Génome et Environnement (UMR CNRS 6023), Clermont Université Blaise Pascal,

Complexe Scientifique des Cézeaux, 24 Avenue des Landais, BP 80026, 63171 Aubière Cedex, FranceABSTRACT: The impact of fish and oysters on components of the pelagic microbial food web

(MFW) was studied in a mesocosm experiment using Mediterranean coastal waters. Two mesocosms contained natural water only (‘Controls"), 2 contained natural water with Crassostrea gigas(‘Oyster"), and 2 contained natural water with Atherinaspp. (‘Fish"). Abundances and biomasses of microorganisms (viruses, bacteria, phytoplankton, heterotrophic flagellates, and ciliates) were measured to estimate their contribution to the total microbial carbon biomass. Two MFW indices, the microbial autotroph:heterotroph C biomass ratio (A:H) structural index and the gross primary production:respiration ratio (GPP:R) functional index, were defined. In the Fish mesocosms, selective predation on zooplankton led to a trophic cascade with 51% higher phyto- plankton C biomass and consequently higher A:H and GPP:R than in the Controls. By the end of the experiment, the Oyster mesocosms had a bacterial C biomass 87% higher and phytoplankton C biomass 93% lower than the Controls, giving significantly lower A:H and GPP:R (<1). Overall, the results showed that wild zooplanktivorous fish had a cascading trophic effect, making the MFW more autotrophic (both indices >1), whereas oyster activities made the MFW more hetero- trophic (both indices <1). These MFW indices can therefore be used to assess the impact of multi- ple local and global forcing factors on the MFW. The results presented here also have implications for sustainable management of coastal environments, suggesting that intense cultivation of filter feeders can be coupled with management to encourage wild local zooplanktivorous fishes to maintain a more resilient system and preserve the equilibrium of the MFW.

KEY WORDS: Microbial food web · Virioplankton · Bacterioplankton · Phytoplankton · Protozooplankton · Crassostrea · Atherina· Autotrophy · Heterotrophy

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Mar Ecol Prog Ser 535: 11-27, 201512

microorganisms within the MFW (heterotrophic bacteria, flagellates, ciliates, phytoplankton, and viruses) and between the MFW and multicellular organisms at higher trophic levels (Mostajir et al.

2015). The strength of these interactions in the pe -

lagic MFW can be modified by natural and anthro- pogenic chemical, physical, and biological forcing factors, leading to changes in MFW structure and functioning. There have been numerous investiga- tions on the effects of chemical and physical forcing factors such as acidification (Riebesell et al. 2013), water warming (Vidussi et al. 2011, Fouilland et al.

2013, von Scheibner et al. 2014), nutrient loading by

flood events (Pecqueur et al. 2011), and ultraviolet- B radiation (Mostajir et al. 1999, Vidussi et al. 2011) on specific components of the MFW, or on the MFW in general. However, few studies, particularly in seawater, have focused on the responses of the

MFW to top-down alterations. For instance, most

studies of the effects of mariculture (shellfish and fish farms) in coastal zones have focused on the feeding regimes of cultured bivalves or fish to de - termine the organisms that contribute to their diet. Most studies found that bivalves, especially oysters, exerted top-down control on phytoplankton (Newell et al. 2007), but some showed that oysters grazed mainly on non-chlorophyllous particles (Charpy et al. 2012) or heterotrophic micro organisms (Dupuy et al. 2000). It has been established that fish predation can control the plankton community efficiently, and this biotic top-down control has been used since the

1980s to regulate primary production in lakes (Car-

penter et al. 1987).

However, few studies have considered the effects

of mariculture (shellfish and fish farms) on the struc- ture and functioning of the MFW as a whole in an integrated way. Cultivated oysters are important anthropogenic biological forcing factors in coastal waters and, like fish, can be considered top predators of MFW components. The 2 animals selected for this experiment have different feeding strategies: the oyster Crassostrea gigasis a non-selective filter feeder cultivated in many farms in various coastal waters, and local wild sand smelt (Atherinaspp.) is a selective zooplanktivore which is widespread in the Mediterranean and other adjacent seas as well as in Mediterranean lagoons. This study set out to deter- mine (1) how oysters and fish as top predators change the abundance and biomass of all communi- ties in the MFW, (2) whether these changes influence the structure of the MFW, and (3) whether there are simultaneous changes in the structure and function- ing of the MFW.MATERIALS AND METHODS

Experimental site

The mesocosm experiment was carried out at the

Mediterranean center for Marine Ecosystem Experi-

mental Research (MEDIMEER) (www.medimeer. univ-montp2.fr/) based at the marine station of Sète (SMEL, University of Montpellier 2, 43°24"49"N,

3°41"19"E).

The mesocosms were immersed in the Thau

lagoon on the French Mediterranean coast. In - tensive shellfish farms (oysters and mussels) cover about one-fifth of the lagoon area, and the lagoon provides 10% of French oyster production (Souchu et al. 1998). The Thau watershed covers an area of 280 km 2 . Thau is not a deep lagoon (maximum depth 10 m, average depth 4.5 m), and there are large variations in salinity (be - tween 24 and 38) and water temperature (from 4 to 27°C). Concentrations of nutrients in the Thau lagoon are relatively low (nitrate concentrations <1 µM), although they can increase after flood events.

Experimental design and mesocosms

Six mesocosms (maximum water depth of 2 m)

were moored near the MEDIMEER pontoon on 26

October 2005 (Day 0). Natural lagoon surface

water was filtered through a 1000 µm mesh sieve and after pooling was used to simultaneously fill all mesocosms to a final volume of 2260 l for each mesocosm. Note that these pelagic mesocosms mimic only the natural water column without including the sediment. Two of the mesocosms contained natural water (‘Control"), 2 contained natural water with 10 Crassostrea gigas(‘Oyster"), and 2 contained natural water with 29 Atherina (‘Fish"). The water column in each mesocosm was continuously mixed by a pump (Iwaki MD30MX) to ensure that the conditions were uniform and to avoid particle settling. The mesocosms were not refilled after each sampling, and the flow rate of the pumps used for mixing the water column of the mesocosms was adjusted using an ultrasonic flowmeter (Minisonic P, Ultraflux) to ensure a turn- over of the whole water mass within the mesocosm every 1 h, taking into account the reduction of total volume due to daily sampling. Detailed infor- mation about the mesocosms can be found in

Nouguier et al. (2007).

Mostajir et al.: Microbial food web responses to top predators

Capture of oysters and fish and acclimation

Oysters were collected by divers in the Thau

lagoon on 17 October 2005 and kept in an 80 l container continuously supplied with lagoon water.

Before the oysters were introduced into the meso-

cosms, they were brushed to eliminate any organ- isms adhering to their valves. From 26 to 27 Octo- ber, they were acclimated in 0.2 µm filtered lagoon water (Whatman, 0.8 and 0.2 µm) and oxy- genized continuously by bubbling. To check that the oysters were alive throughout the experiment, the frequency of valve opening during the experi- ment was continuously monitored. To do this, 2

PVC shelves were constructed, each with 2 rows

of 5 plates, and 10 oysters were fixed to each shelf. One shelf was placed in each of the 2 Oyster mesocosms in the afternoon on 27 October 2005 (Day 1). At the same time, dummy shelves of the same material and structure but without oysters were placed in the other 4 mesocosms (Control and Fish mesocosms) to provide the same amount of shade as in the Oyster mesocosms. Each shelf (Fig. 1A) was fitted with a measurement system consisting of an arm attached to the top shell of each oyster to amplify the valve movement, with a

Hall effect sensor on the shelf and a magnet on

the arm (Mostajir et al. 2012). The output voltage from the sensor, which depended on the gape, was recorded every 2 s by a data logger (CR23X,

Campbell Sci entific). The data were averaged and

saved every 5 min. Monitoring the oyster gape confirmed that all 20 oysters remained alive during the experiment. As an example, the gape measurement of one of the oysters during the experiment is illustrated in Fig. 1B, which shows that it was open continuously at the beginning of the experiment, indicating continuous feeding. Towards the end of the experiment, oyster filtering became irregular, with periods when the oyster was closed.

Pelagic fish (sand smelt, n = 200) were caught

using a fish net on 3 October 2005 in several different localities in the Thau lagoon and adjacent basins and kept in an 80 l container continuously supplied with lagoon water. From 26 to 27 October, the fish were acclimated in 0.2 µm filtered lagoon water (PALL fil- ter, 0.8 and 0.2 µm) and oxygenized continuously by bubbling. Fish (n = 29) were placed in each of 2 mesocosms on 27 October 2005 (Day 1; Fish meso- cosms). The fish were caught at the end of the exper- iment, and 28 fish in each of the duplicate mesocosms were found still alive. 13 Fig. 1. (A) Shelf with 2 rows of 5 plates for simultaneously monitoring the gapes of 10 oystersCrassostrea gigasduring the experiment using a measurement system consisting of an arm, a magnet, and a sensor. (B) Data on the gape of one of the oysters, averaged and stored every 5 min, showing the gape on most of Days 2 and 3 and the period when the oyster was sometimes closed at the end of the experiment (Days 8 and 9)

Mar Ecol Prog Ser 535: 11-27, 201514

Light, temperature, and salinity

Incident PAR was monitored every 10 min between

14:00 h on Day 1 (27 October) and 23:50 h on Day 8

(3 November) using a spectroradiometer (TriOS

RAMSES ACC hyperspectral) connected to a Camp-

bell Scientific data logger (CR23X), as described by

Nouguier et al. (2007). The water temperature in

each mesocosm was measured every 5 min by Camp- bell Scientific 107 temperature probes situated at 3 depths in the mesocosms (0.4, 0.8, and 1.2 m). For each probe, the data were averaged and recorded every 10 min. The salinity in all mesocosms was measured every day between 10:00 and 11:00 h using a WTW 197i conductivity meter.

Mesocosm sampling

When all mesocosms had been filled and the water

column in each mesocosm had been mixed for 1 h using the pump in each mesocosm, a 20 l sample was taken using a pump (Iwaki MD30MX) from one of the control mesocosms to characterize the initial water conditions on Day 0. Samples were taken once a day at 10:00 h from Day 1 until the end of the exper- iment (Day 9) to measure nutrients and dissolved organic carbon as well as the abundances of virus- like particles (VLPs), heterotrophic bacteria, and chlorophyll concentrations.

Samples were taken from all mesocosms on Days 1,

3, 5, 7, and 9 between 10:00 and 11:00 h to measure

the net oxygen production rates, plankton com munity respiration, and abundances of heterotrophic flagel- lates, ciliates (samples were also taken on Day 2), and larger zooplankton (samples were not taken on Day 5). The gross oxygen production was estimated from net community production and res piration.

Nutrients

Samples for nitrite and nitrate (NO

2- +NO 3- ), phos- phate (PO 43-
), and silicate (SiO 44-
) analysis were col- lected in acid-washed polyethylene bottles. Samples were vacuum filtered (<20 kPa) onto precombusted GF/F filters using pre-rinsed polycarbonate filter hold- ers (Nalgene). Filtered sub-samples for NO 2- +NO 3- and PO 43-
analysis were stored frozen (-20°C) in

125 ml borosilicate bottles. Filtered sub-samples for

SiO 44-
analysis were stored at 4°C in 125 ml polyeth- ylene bottles. Samples for dissolved nutrients were

subsequently analyzed using a standard automatedcolorimetric method (Wood et al. 1967, Tréguer & Le

Corre 1975) on a segmented flow Bran Luebbe auto-

analyzer II. NH 4 concentration was not included in the dissolved nitrogen (NO 3 +NO 2 ) concentrations due to methodological problems.

Dissolved organic carbon (DOC)

To measure DOC, mesocosm samples collected in

glass bottles were filtered through GF/F filters into

10 ml Pyrex tubes (all materials were pre-combusted

at 450°C for 6 h), immediately acidified with 85% H 3 PO 4 (final pH ~2), and stored at 4°C in the dark.

The DOC concentration was measured using a Shi-

madzu TOC-5000 total carbon analyzer with 1.2% platinum-coated silica pillows as a catalyst (Sohrin & Sempéré 2005). The DOC concentration calculation was obtained from peak areas and a 4-point calibra- tion curve obtained daily by injecting working solu- tions of acidified (with H 3 PO 4 ) potassium hydrogen phthalate that were freshly prepared every by diluting the stock solution with Milli-Q water. The running blank was subtracted from the average peak area of the samples (n = 3 or 4) divided by the slope of the calibration curve. The running blank was de - termined as the average of all peak areas of the Milli-

Q water acidified with H

3 PO 4 . The acidified Milli-Q water was injected in triplicate every 4 samples. To ensure the accuracy and the stability of the DOC analysis, low-carbon water and deep seawater refer- ence distributed by the laboratory of D. Hansell (Uni- versity of Miami, USA) were measured daily.

Net oxygen production, dark oxygen respiration,

and gross oxygen production

To measure the oxygen production and respiration,

12 borosilicate bottles (120 ml each) were carefully

filled from each 20 l sampling carboy using a silicone rubber tube. Four bottles were immediately fixed (time 0) using reagents prepared as described by Caritt & Carpenter (1966). In order to measure the net oxygen production (net community production: NCP), 4 other bottles were wrapped in a piece of the plastic sheet used for constructing the mesocosms and incubated in surface waters of the Thau Lagoonquotesdbs_dbs31.pdfusesText_37

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